Abstract
Vanadate, an inhibitor of phosphotyrosyl phosphatases that exerts insulin-like effects in intact cells, stimulated both maturation and glucose uptake in isolated Xenopus laevis oocytes. Vanadate enhanced the effects of insulin/IGF-I and progesterone on maturation in a dose-dependent manner, with an effective concentration of 750 microM and a maximum at 2 mM, whereas, in the absence of hormone, activation of maturation was seen at 10 mM vanadate. Further, vanadate at 2 mM increased glucose uptake, but this effect was not additive to that of the hormone. In cell-free systems, vanadate caused a 12-fold stimulation of autophosphorylation of the oocyte IGF-I receptor in the absence, but not in the presence, of IGF-I and inhibited largely, but not totally, receptor dephosphorylation induced by an extract of oocytes rich in phosphotyrosyl phosphatase activities. These effects were dose dependent, with effective concentrations of 50-100 microM and maxima at 2 mM. Moreover, using an acellular assay to study the effect of vanadate on the activation of maturation promoting factor (MPF), we found that vanadate at 2 mM stimulated the activation of the MPF H1 kinase. This suggests that vanadate did not prevent dephosphorylation of p34cdc2 on tyrosine residues. Vanadate thus exerted insulin-like effects in oocytes, including stimulation of maturation. These effects might result from a direct or indirect action of vanadate on the IGF-I receptor kinase and on MPF activity.
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Selected References
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- Boivin P., Galand C. The human red cell acid phosphatase is a phosphotyrosine protein phosphatase which dephosphorylates the membrane protein band 3. Biochem Biophys Res Commun. 1986 Jan 29;134(2):557–564. doi: 10.1016/s0006-291x(86)80456-9. [DOI] [PubMed] [Google Scholar]
- Brautigan D. L., Bornstein P., Gallis B. Phosphotyrosyl-protein phosphatase. Specific inhibition by Zn. J Biol Chem. 1981 Jul 10;256(13):6519–6522. [PubMed] [Google Scholar]
- Brautigan D. L., Sunwoo J., Labbé J. C., Fernandez A., Lamb N. J. Cell cycle oscillation of phosphatase inhibitor-2 in rat fibroblasts coincident with p34cdc2 restriction. Nature. 1990 Mar 1;344(6261):74–78. doi: 10.1038/344074a0. [DOI] [PubMed] [Google Scholar]
- Brown D. J., Gordon J. A. The stimulation of pp60v-src kinase activity by vanadate in intact cells accompanies a new phosphorylation state of the enzyme. J Biol Chem. 1984 Aug 10;259(15):9580–9586. [PubMed] [Google Scholar]
- Brunati A. M., Pinna L. A. Isolation and partial characterization of distinct species of phosphotyrosyl protein phosphatases from rat spleen. Biochem Biophys Res Commun. 1985 Dec 31;133(3):929–936. doi: 10.1016/0006-291x(85)91225-2. [DOI] [PubMed] [Google Scholar]
- Cantley L. C., Jr, Aisen P. The fate of cytoplasmic vanadium. Implications on (NA,K)-ATPase inhibition. J Biol Chem. 1979 Mar 25;254(6):1781–1784. [PubMed] [Google Scholar]
- Carpenter G. Vanadate, epidermal growth factor and the stimulation of DNA synthesis. Biochem Biophys Res Commun. 1981 Oct 30;102(4):1115–1121. doi: 10.1016/s0006-291x(81)80127-1. [DOI] [PubMed] [Google Scholar]
- Cicirelli M. F., Pelech S. L., Krebs E. G. Activation of multiple protein kinases during the burst in protein phosphorylation that precedes the first meiotic cell division in Xenopus oocytes. J Biol Chem. 1988 Feb 5;263(4):2009–2019. [PubMed] [Google Scholar]
- Cicirelli M. F., Tonks N. K., Diltz C. D., Weiel J. E., Fischer E. H., Krebs E. G. Microinjection of a protein-tyrosine-phosphatase inhibits insulin action in Xenopus oocytes. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5514–5518. doi: 10.1073/pnas.87.14.5514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cyert M. S., Kirschner M. W. Regulation of MPF activity in vitro. Cell. 1988 Apr 22;53(2):185–195. doi: 10.1016/0092-8674(88)90380-7. [DOI] [PubMed] [Google Scholar]
- Deshpande A. K., Kung H. F. Insulin induction of Xenopus laevis oocyte maturation is inhibited by monoclonal antibody against p21 ras proteins. Mol Cell Biol. 1987 Mar;7(3):1285–1288. doi: 10.1128/mcb.7.3.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dubyak G. R., Kleinzeller A. The insulin-mimetic effects of vanadate in isolated rat adipocytes. Dissociation from effects of vanadate as a (Na+-K+)ATPase inhibitor. J Biol Chem. 1980 Jun 10;255(11):5306–5312. [PubMed] [Google Scholar]
- Dunphy W. G., Newport J. W. Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase. Cell. 1989 Jul 14;58(1):181–191. doi: 10.1016/0092-8674(89)90414-5. [DOI] [PubMed] [Google Scholar]
- Félix M. A., Cohen P., Karsenti E. Cdc2 H1 kinase is negatively regulated by a type 2A phosphatase in the Xenopus early embryonic cell cycle: evidence from the effects of okadaic acid. EMBO J. 1990 Mar;9(3):675–683. doi: 10.1002/j.1460-2075.1990.tb08159.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gautier J., Matsukawa T., Nurse P., Maller J. Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle. Nature. 1989 Jun 22;339(6226):626–629. doi: 10.1038/339626a0. [DOI] [PubMed] [Google Scholar]
- Gautier J., Minshull J., Lohka M., Glotzer M., Hunt T., Maller J. L. Cyclin is a component of maturation-promoting factor from Xenopus. Cell. 1990 Feb 9;60(3):487–494. doi: 10.1016/0092-8674(90)90599-a. [DOI] [PubMed] [Google Scholar]
- Goris J., Hermann J., Hendrix P., Ozon R., Merlevede W. Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. FEBS Lett. 1989 Mar 13;245(1-2):91–94. doi: 10.1016/0014-5793(89)80198-x. [DOI] [PubMed] [Google Scholar]
- Gould K. L., Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 1989 Nov 2;342(6245):39–45. doi: 10.1038/342039a0. [DOI] [PubMed] [Google Scholar]
- Hainaut P., Kowalski A., Giorgetti S., Baron V., Van Obberghen E. Insulin and insulin-like-growth-factor-I (IGF-I) receptors in Xenopus laevis oocytes. Comparison with insulin receptors from liver and muscle. Biochem J. 1991 Feb 1;273(Pt 3):673–678. doi: 10.1042/bj2730673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huchon D., Ozon R., Demaille J. G. Protein phosphatase-1 is involved in Xenopus oocyte maturation. Nature. 1981 Nov 26;294(5839):358–359. doi: 10.1038/294358a0. [DOI] [PubMed] [Google Scholar]
- Janicot M., Lane M. D. Activation of glucose uptake by insulin and insulin-like growth factor I in Xenopus oocytes. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2642–2646. doi: 10.1073/pnas.86.8.2642. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klarlund J. K. Transformation of cells by an inhibitor of phosphatases acting on phosphotyrosine in proteins. Cell. 1985 Jul;41(3):707–717. doi: 10.1016/s0092-8674(85)80051-9. [DOI] [PubMed] [Google Scholar]
- Korn L. J., Siebel C. W., McCormick F., Roth R. A. Ras p21 as a potential mediator of insulin action in Xenopus oocytes. Science. 1987 May 15;236(4803):840–843. doi: 10.1126/science.3554510. [DOI] [PubMed] [Google Scholar]
- Labbé J. C., Picard A., Karsenti E., Dorée M. An M-phase-specific protein kinase of Xenopus oocytes: partial purification and possible mechanism of its periodic activation. Dev Biol. 1988 May;127(1):157–169. doi: 10.1016/0012-1606(88)90197-2. [DOI] [PubMed] [Google Scholar]
- Lau K. H., Farley J. R., Baylink D. J. Phosphotyrosyl protein phosphatases. Biochem J. 1989 Jan 1;257(1):23–36. doi: 10.1042/bj2570023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Le Goascogne C., Hirai S., Baulieu E. E. Induction of germinal vesicle breakdown in Xenopus laevis oocytes: synergistic action of progesterone and insulin. J Endocrinol. 1984 Apr;101(1):7–12. doi: 10.1677/joe.0.1010007. [DOI] [PubMed] [Google Scholar]
- Leis J. F., Kaplan N. O. An acid phosphatase in the plasma membranes of human astrocytoma showing marked specificity toward phosphotyrosine protein. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6507–6511. doi: 10.1073/pnas.79.21.6507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lichtstein D., Mullikin-Kilpatrick D., Blume A. J. Modification of neuroblastoma x glioma hybrid NG108-15 adenylate cyclase by vanadium ions. Biochem Biophys Res Commun. 1982 Apr 14;105(3):1157–1165. doi: 10.1016/0006-291x(82)91091-9. [DOI] [PubMed] [Google Scholar]
- Maller J. L., Koontz J. W. A study of the induction of cell division in amphibian oocytes by insulin. Dev Biol. 1981 Jul 30;85(2):309–316. doi: 10.1016/0012-1606(81)90262-1. [DOI] [PubMed] [Google Scholar]
- Maller J. L., Krebs E. G. Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3':5'-monophosphate-dependent protein kinase. J Biol Chem. 1977 Mar 10;252(5):1712–1718. [PubMed] [Google Scholar]
- Maller J. L. Xenopus oocytes and the biochemistry of cell division. Biochemistry. 1990 Apr 3;29(13):3157–3166. doi: 10.1021/bi00465a001. [DOI] [PubMed] [Google Scholar]
- Masui Y., Markert C. L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool. 1971 Jun;177(2):129–145. doi: 10.1002/jez.1401770202. [DOI] [PubMed] [Google Scholar]
- Meyerovitch J., Farfel Z., Sack J., Shechter Y. Oral administration of vanadate normalizes blood glucose levels in streptozotocin-treated rats. Characterization and mode of action. J Biol Chem. 1987 May 15;262(14):6658–6662. [PubMed] [Google Scholar]
- Morgan D. O., Kaplan J. M., Bishop J. M., Varmus H. E. Mitosis-specific phosphorylation of p60c-src by p34cdc2-associated protein kinase. Cell. 1989 Jun 2;57(5):775–786. doi: 10.1016/0092-8674(89)90792-7. [DOI] [PubMed] [Google Scholar]
- Morla A. O., Draetta G., Beach D., Wang J. Y. Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell. 1989 Jul 14;58(1):193–203. doi: 10.1016/0092-8674(89)90415-7. [DOI] [PubMed] [Google Scholar]
- Mustelin T., Coggeshall K. M., Altman A. Rapid activation of the T-cell tyrosine protein kinase pp56lck by the CD45 phosphotyrosine phosphatase. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6302–6306. doi: 10.1073/pnas.86.16.6302. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Norbury C. J., Nurse P. Control of the higher eukaryote cell cycle by p34cdc2 homologues. Biochim Biophys Acta. 1989 Jul 28;989(1):85–95. doi: 10.1016/0304-419x(89)90036-x. [DOI] [PubMed] [Google Scholar]
- Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. doi: 10.1038/344503a0. [DOI] [PubMed] [Google Scholar]
- Rime H., Ozon R. Protein phosphatases are involved in the in vivo activation of histone H1 kinase in mouse oocyte. Dev Biol. 1990 Sep;141(1):115–122. doi: 10.1016/0012-1606(90)90106-s. [DOI] [PubMed] [Google Scholar]
- Roy L. M., Singh B., Gautier J., Arlinghaus R. B., Nordeen S. K., Maller J. L. The cyclin B2 component of MPF is a substrate for the c-mos(xe) proto-oncogene product. Cell. 1990 Jun 1;61(5):825–831. doi: 10.1016/0092-8674(90)90192-h. [DOI] [PubMed] [Google Scholar]
- Russell P., Nurse P. The mitotic inducer nim1+ functions in a regulatory network of protein kinase homologs controlling the initiation of mitosis. Cell. 1987 May 22;49(4):569–576. doi: 10.1016/0092-8674(87)90459-4. [DOI] [PubMed] [Google Scholar]
- Ryder J. W., Gordon J. A. In vivo effect of sodium orthovanadate on pp60c-src kinase. Mol Cell Biol. 1987 Mar;7(3):1139–1147. doi: 10.1128/mcb.7.3.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shenoy S., Choi J. K., Bagrodia S., Copeland T. D., Maller J. L., Shalloway D. Purified maturation promoting factor phosphorylates pp60c-src at the sites phosphorylated during fibroblast mitosis. Cell. 1989 Jun 2;57(5):763–774. doi: 10.1016/0092-8674(89)90791-5. [DOI] [PubMed] [Google Scholar]
- Solomon M. J., Glotzer M., Lee T. H., Philippe M., Kirschner M. W. Cyclin activation of p34cdc2. Cell. 1990 Nov 30;63(5):1013–1024. doi: 10.1016/0092-8674(90)90504-8. [DOI] [PubMed] [Google Scholar]
- Tamura S., Brown T. A., Dubler R. E., Larner J. Insulin-like effect of vanadate on adipocyte glycogen synthase and on phosphorylation of 95,000 dalton subunit of insulin receptor. Biochem Biophys Res Commun. 1983 May 31;113(1):80–86. doi: 10.1016/0006-291x(83)90434-5. [DOI] [PubMed] [Google Scholar]
- Tamura S., Brown T. A., Whipple J. H., Fujita-Yamaguchi Y., Dubler R. E., Cheng K., Larner J. A novel mechanism for the insulin-like effect of vanadate on glycogen synthase in rat adipocytes. J Biol Chem. 1984 May 25;259(10):6650–6658. [PubMed] [Google Scholar]
- Tonks N. K., Cicirelli M. F., Diltz C. D., Krebs E. G., Fischer E. H. Effect of microinjection of a low-Mr human placenta protein tyrosine phosphatase on induction of meiotic cell division in Xenopus oocytes. Mol Cell Biol. 1990 Feb;10(2):458–463. doi: 10.1128/mcb.10.2.458. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vera J. C., Rosen O. M. Functional expression of mammalian glucose transporters in Xenopus laevis oocytes: evidence for cell-dependent insulin sensitivity. Mol Cell Biol. 1989 Oct;9(10):4187–4195. doi: 10.1128/mcb.9.10.4187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vitto A., Jr, wallace R. A. Maturation of Xenopus oocytes. I. Facilitation by ouabain. Exp Cell Res. 1976 Jan;97:56–62. doi: 10.1016/0014-4827(76)90654-6. [DOI] [PubMed] [Google Scholar]
- Wallace R. A., Misulovin Z. The role of zinc and follicle cells in insulin-initiated meiotic maturation of Xenopus laevis oocytes. Science. 1980 Nov 21;210(4472):928–930. doi: 10.1126/science.7001631. [DOI] [PubMed] [Google Scholar]
- Wu M., Gerhart J. C. Partial purification and characterization of the maturation-promoting factor from eggs of Xenopus laevis. Dev Biol. 1980 Oct;79(2):465–477. doi: 10.1016/0012-1606(80)90131-1. [DOI] [PubMed] [Google Scholar]